NEURONAL-ACTIVITY IN THE IPSILATERAL VESTIBULAR NUCLEUS FOLLOWING UNILATERAL LABYRINTHECTOMY IN THE ALERT GUINEA-PIG

1. Neuronal activity was investigated in the left superior vestibular nucleus (SVN), lateral vestibular nucleus (LVN), and rostral part of t he medial vestibular nucleus (MVN) in the alert guinea pig after a uni lateral (left) labyrinthectomy was performed. Vestibular neurons were recorded either immediately (just-postoperative group, n = 6) or 1 wk after labyrinthectomy (1-wk-postoperative group, n = 6) and compared w ith the activity recorded in intact animals (control group, n = 6). 2. Animals were prepared for extracellular recording of single-unit acti vity and for eye movement recording (scleral search coil technique). T o enable stimulation of the left vestibular nerve, bipolar silver ball electrodes were chronically implanted either in contact with the bony labyrinth in the control group or close to the stump of the vestibula r nerve after labyrinthectomy. Complete labyrinthectomy was performed under halothane anesthesia. 3. The criterion used to select vestibular neurons for analysis was their recruitment by an electric shock on th e vestibular nerve. Of the 589 recorded neurons, 424, defined as secon d-order vestibular neurons, were recruited at monosynaptic latencies ( 0.85-1.15 ms) and 165 were recruited at polysynaptic latencies. One hu ndred three second-order vestibular neurons were recorded in the contr ol group, 173 in the just-postoperative group, and 148 in the 1-wk-pos toperative group. 4. The activity of the electrically recruited neuron s was recorded during sinusoidal horizontal head rotation in the dark (0.3 Hz, 40 degrees/s peak velocity). The behavior of the neurons was analyzed by plotting their firing rate against head velocity. The Y-in tercept of the regression line was used to express spontaneous firing rate (resting discharge), and its slope was used to express the sensit ivity of the neuron-to-head velocity. 5. In the absence of statistical ly significant difference between the characteristics of the neuronal discharge of the second-order vestibular neurons recorded in the SVN, LVN, and rostral MVN, the data were pooled. The Resting discharge of t hese cells amounted to 41.0 +/- 24.7 (SD) spikes/s in the control stat e, fell to 7.2 +/- 13.9 spikes/s just after labyrinthectomy, and compl etely returned to normal values 1 wk after surgery (42.5 +/- 21.6 spik es/s). Among the monosynaptically recruited neurons, the percentage of silent units was 0% in the control group, 69% in the just-postoperati ve group, and 0% in the 1-wk-postoperative group. 6. By contrast, the sensitivity to head velocity of the second-order vestibular neurons, w hich was 0.69 +/- 0.48 (SD) spikes . s(-1)/deg . s(-1) in the control state and which fell to 0.03 +/- 0.11 spikes . s(-1)/deg . s(-1) just after labyrinthectomy, remained low 1 wk after injury (0.21 +/- 0.26 s pikes . s(-1)/deg . s(-1)). Moreover, the slight recovery of sensitivi ty to head rotation was due only to units behaving as type II neurons. 7. The mean resting discharge of the polysynaptically recruited neuro ns (pooled from the 3 explored nuclei) was 31.6 +/- 19.3 spikes/s in t he control group. It decreased to 11.6 +/- 12.1 spikes/s in the just-p ostoperative group and recovered to 39.8 +/- 20.2 spikes/s in the l-wk -postoperative group. No neuron was silent at rest either in the contr ol group or in the 1-wk-postoperative group. Just after labyrinthectom y, 35% of the neurons had a null resting activity. The mean sensitivit y to head velocity of these neurons was 0.55 +/- 0.42 spikes . s(-1)/d eg . s(-1) in the control group. It decreased to 0.05 +/- 0.12 spikes . s(-1)/deg . s(-1) in the just-postoperative group and recovered to 0 .22 +/- 0.17 spikes . s(-1)/deg . s(-1) in the 1-wk-postoperative grou p. 8. We conclude that, at least in the guinea pig, the restoration of the spontaneous activity of the deafferented neurons is complete 1 wk after a unilateral labyrinthectomy and thus probably plays an importa nt role in vestibular compensation. Moreover, the difference seen betw een the complete recovery of the resting discharge and the absence of recovery of sensitivity to head velocity 1 wk after the lesion is furt her evidence that compensation of static vestibular symptoms and dynam ic symptoms are mediated by two completely distinct mechanisms.